Abstract
Grandparents in rural Appalachia with primary caregiving responsibilities for their grandchildren often struggle with high levels of stress, inadequate resources, and poor physical and mental health. However, implications for children of being raised by grandparents rarely have been examined, particularly in terms of stress biomarkers. The present study investigated salivary C-reactive protein, interleukin-6, and tumor necrosis factor alpha in a small sample of children (N = 20) aged 5 to 18 years being reared by grandparents in two rural counties in Kentucky, a region well known for its resource scarcity. Saliva samples were collected from children 30 min after waking at two time points spaced one year apart. Grandparents and children completed a series of questionnaires via interview. Children’s internalizing symptoms were related to greater markers of inflammation over time. Grandparent stress and poor mental health were also related to greater inflammation, while grandparent positive parenting and religiosity were associated with lower inflammation.
Similar content being viewed by others
References
Administration for Children and Families (2014) Child Maltreatment 2014. Available from http://www.acf.hhs.gov/programs/cb/research-data-technology/statistics-research/child-maltreatment Accessed 12 April 2017.
Appalachian Regional Commission. (2014) The Appalachian Region: A Data Overview from the 2008-2012 American Community Survey. 2014; http://www.arc.gov/research/researchreportdetails.asp?REPORT_ID=109.
Behringer, B., & Friedell, G. H. (2006). Appalachia: where place matters in health. Preventing Chronic Disease, 3(4).
Beijers, R., Riksen-Walraven, J. M., & de Weerth, C. (2013). Cortisol regulation in 12-month-old human infants: associations with the infants' early history of breastfeeding and co-sleeping. Stress, 16(3), 267–277.
Bellavance, M. A., & Rivest, S. (2014). The HPA–immune axis and the immunomodulatory actions of glucocorticoids in the brain. Frontiers in Immunology, 5, 136.
Berry, J. O., & Jones, W. H. (1995). The parental stress scale: Initial psychometric evidence. Journal of Social and Personal Relationships, 12, 463–472.
Black, P. H., & Garbutt, L. D. (2002). Stress, inflammation and cardiovascular disease. Journal of Psychosomatic Research, 52(1), 1–23.
Blair, C., Raver, C. C., Granger, D., Mills-Koonce, R., Hibel, L., & Investigators, F. L. P. K. (2011). Allostasis and allostatic load in the context of poverty in early childhood. Development and Psychopathology, 23(3), 845–857.
Carlsson, E., Frostell, A., Ludvigsson, J., & Faresjo, M. (2014). Psychological stress in children may alter the immune response. The Journal of Immunology, 192, 2071–2081.
Cassidy, J., & Shaver, P. R. (Eds.). (2002). Handbook of attachment: Theory, research, and clinical applications. Rough Guides.
Chen, X. K., Wen, S. W., Fleming, N., Demissie, K., Rhoads, G. G., & Walker, M. (2007). Teenage pregnancy and adverse birth outcomes: a large population based retrospective cohort study. International Journal of Epidemiology, 36(2), 368–373.
Chorpita, B. F., Tracey, S. A., Brown, T. A., Collica, T. J., & Barlow, D. H. (1997). Assessment of worry in children and adolescents: An adaptation of the Penn State Worry Questionnaire. Behavior Research and Therapy, 35, 569–581.
Chrousos, G. P. (2000). Stress, chronic inflammation, and emotional and physical well-being: concurrent effects and chronic sequelae. Journal of Allergy and Clinical Immunology, 106(5), S275–S291.
Clark, C. R., Coull, B., Berkman, L. F., Buring, J. E., & Ridker, P. M. (2011). Geographic variation in cardiovascular inflammation among healthy women in the Women's Health Study. PLoS One, 6(11), e27468.
Collins, D., Abadi, M. H., Johnson, K., Shamblen, S., & Thompson, K. (2011). Non-medical use of prescription drugs among youth in an Appalachian population: Prevalence, predictors, and implications for prevention. Journal of Drug Education, 41(3), 309–326.
Conger, R. D., & Donnellan, M. B. (2007). An interactionist perspective on the socioeconomic context of human development. Annual Review of Psychology, 58, 175–199.
Conger, R. D., Schofield, T. J., & Neppl, T. K. (2012). Intergenerational continuity and discontinuity in harsh parenting. Parenting, 12(2–3), 222–231.
Connor-Smith, J. K., Compas, B. E., Wadsworth, M. E., Thomsen, A. H., & Saltzman, H. (2000). Responses to stress in adolescence: measurement of coping and involuntary stress responses. Journal of Consulting and Clinical Psychology, 68, 976.
Delves, P. J., Martin, S. J., Burton, D. R., & Roitt, I. M. (2017). Essential immunology. John Wiley & Sons.
Downie, J. M., Hay, D. A., Horner, B. J., Wichmann, H., & Hislop, A. L. (2010). Children living with their grandparents: resilience and wellbeing. International Journal of Social Welfare, 19, 8–22.
Efron, B., & Tibshirani, R. J. (1994). An introduction to the bootstrap. CRC press.
Espinosa-Oliva, A. M., De Pablos, R. M., Villarán, R. F., Argüelles, S., Venero, J. L., Machado, A., & Cano, J. (2011). Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiology of Aging, 32(1), 85–102.
Fendrich, M., Weissman, M. M., & Warner, V. (1990). Screening for depressive disorder in children and adolescents: validating the center for epidemiologic studies depression scale for children. American Journal of Epidemiology, 131, 538–551.
Gabay, C. (2006). Interleukin-6 and chronic inflammation. Arthritis Research & Therapy, 8(2), S3.
Gaur, U., & Aggarwal, B. B. (2003). Regulation of proliferation, survival and apoptosis by members of the TNF superfamily. Biochemical Pharmacology, 66(8), 1403–1408.
Goenka, A., & Kollmann, T. R. (2015). Development of immunity in early life. Journal of Infection, 71, 112–120.
Goodman, S. H., Rouse, M. H., Connell, A. M., Broth, M. R., Hall, C. M., & Heyward, D. (2011). Maternal depression and child psychopathology: a meta-analytic review. Clinical Child and Family Psychology Review, 14(1), 1–27.
Granger, D. A., Kivlighan, K. T., Fortunato, C., Harmon, A. G., Hibel, L. C., Schwartz, E. B., & Whembolua, G. L. (2007). Integration of salivary biomarkers into developmental and behaviorally-oriented research: problems and solutions for collecting specimens. Physiology & Behavior, 92(4), 583–590.
Hendryx, M. (2009). Mortality from heart, respiratory, and kidney disease in coal mining areas of Appalachia. International Archives of Occupational and Environmental Health, 82(2), 243–249.
Hendryx, M. (2010). Poverty and mortality disparities in central Appalachia: mountaintop mining and environmental justice. Journal of Health Disparities Research and Practice, 4(3), 44–53.
Hendryx, M., & Innes-Wimsatt, K. A. (2013). Increased risk of depression for people living in coal mining areas of central Appalachia. Ecopsychology, 5(3), 179–187.
Hendryx, M., & Zullig, K. J. (2009). Higher coronary heart disease and heart attack morbidity in Appalachian coal mining regions. Preventive Medicine, 49(5), 355–359.
Hueston, W. J., Geesey, M. E., & Diaz, V. (2008). Prenatal care initiation among pregnant teens in the United States: an analysis over 25 years. Journal of Adolescent Health, 42(3), 243–248.
Izawa, S., Miki, K., Liu, X., & Ogawa, N. (2013). The diurnal patterns of salivary interleukin-6 and C-reactive protein in healthy young adults. Brain, Behavior, and Immunity, 27, 38–41.
Jenkins-Howard, S. B., Stephenson, L., & Mains, M. (2013). Cooperative Extension Nutrition Education Program: Outreach to Southeast Kentucky Families in Poverty. PRISM: A Journal of Regional Engagement, 2(2), 117–132.
Johnson, L. R. (2001). Gastrointestinal Physiology (6th ed.). St. Louis: Mosby.
Jones, L. (1994). Appalachian values. Jesse Stuart Foundation.
Lamers, F., Jonkers, C. C., Bosma, H., Penninx, B. W., Knottnerus, J. A., & van Eijk, J. T. M. (2008). Summed score of the Patient Health Questionnaire-9 was a reliable and valid method for depression screening in chronically ill elderly patients. Journal of Clinical Epidemiology, 61(7), 679–687.
Landgraf, J. M., Abetz, L., & Ware, J. E. (1996). The CHQ User’s Manual. Boston: The Health Institute, New England Medical Center.
Madigan, S., Atkinson, L., Laurin, K., & Benoit, D. (2013). Attachment and internalizing behavior in early childhood: A meta-analysis. Developmental Psychology, 49(4), 672.
Martin, A., Rief, W., Klaiberg, A., & Braehler, E. (2006). Validity of the brief patent health questionnaire mood scale (PHQ-9) in the general population. General Hospital Psychiatry, 28, 71–77.
Martin, C. A., McNeil, D. W., Crout, R. J., Ngan, P. W., Weyant, R. J., Heady, H. R., & Marazita, M. L. (2008). Oral health disparities in Appalachia: Orthodontic treatment need and demand. The Journal of the American Dental Association, 139(5), 598–604.
Matthews, K. A., Chang, Y. F., Thurston, R. C., & Bromberger, J. T. (2014). Child abuse is related to inflammation in mid-life women: role of obesity. Brain, Behavior, and Immunity, 36, 29–34.
McEwen, B. S. (1998). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840(1), 33–44.
Miller, C. S., Foley, J. D., Bailey, A. L., Campell, C. L., Humphries, R. L., Christodoulides, N.…., & McDevitt, J. T. (2010). Current developments in salivary diagnostics. Biomarkers in Medicine, 4, 171–189.
Morey, J. N., Boggero, I. A., Scott, A. B., & Segerstrom, S. C. (2015). Current directions in stress and human immune function. Current Opinion in Psychology, 5, 13–17.
Nonnemaker, J. M., McNeely, C. A., & Blum, R. W. (2003). Public and private domains of religiosity and adolescent health risk behaviors: Evidence from the National Longitudinal Study of Adolescent Health. Social Science & Medicine, 57(11), 2049–2054.
Pepys, M. B., & Hirschfield, G. M. (2003). C-reactive protein: a critical update. Journal of Clinical Investigation, 111(12), 1805.
Pietromonaco, P. R., & Powers, S. I. (2015). Attachment and health-related physiological stress processes. Current Opinion in Psychology, 1, 34–39.
Poehlmann, J., Park, J., Bouffiou, L., Abrahams, J., Shlafer, R., & Hahn, E. (2008). Representations of family relationships in children living with custodial grandparents. Attachment & Human Development, 10(2), 165–188.
Popa, C., Netea, M. G., Van Riel, P. L., van der Meer, J. W., & Stalenhoef, A. F. (2007). The role of TNF-α in chronic inflammatory conditions, intermediary metabolism, and cardiovascular risk. Journal of Lipid Research, 48(4), 751–762.
Puig, J., Englund, M. M., Simpson, J. A., & Collins, W. A. (2013). Predicting adult physical illness from infant attachment: a prospective longitudinal study. Health Psychology, 32(4), 409.
Raine, A., Dodge, K., Loeber, R., Gatzke-Kopp, L., Lynam, D., Reynolds, C.…., & Liu, J. (2006). The reactive-proactive aggression questionnaire: differential correlates of reactive and proactive aggression in adolescent boys. Aggressive Behavior, 32, 159–171.
Raison, C. L., Capuron, L., & Miller, A. H. (2006). Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends in Immunology, 27(1), 24–31.
Schaefer, E. S. (1965). A configurational analysis of children's reports of parent behavior. Journal of Consulting Psychology, 29(6), 552–557.
Schoenberg, N. E., Hatcher, J., & Dignan, M. B. (2008). Appalachian women's perceptions of their community's health threats. The Journal of Rural Health, 24(1), 75–83.
Schumaker, S. A., & Brownell, A. (1984). Toward a theory of social support: Closing conceptual gaps. Journal of Social Issues, 40(4), 11–36.
Segerstrom, S. C., Schipper, L. J., & Greenberg, R. N. (2008). Caregiving, repetitive thought, and immune response to vaccination in older adults. Brain, Behavior, and Immunity, 22(5), 744–752.
Sherbourne, C. D., & Stewart, A. L. (1991). The MOS Social Support Survey. Social Science & Medicine, 32, 705–714.
Slavish, D. C., Graham-Engeland, J. E., Smyth, J. M., & Engeland, C. G. (2015). Salivary markers of inflammation in response to acute stress. Brain, Behavior, and Immunity, 44, 253–269.
Slopen, N., Kubzansky, L. D., McLaughlin, K. A., & Koenen, K. C. (2013). Childhood adversity and inflammatory processes in youth: A prospective study. Psychoneuroendocrinology, 38(2), 188–200.
Smith, G. C., & Hancock, G. R. (2010). Custodial Grandmother-Grandfather Dyads: Pathways Among Marital Distress, Grandparent Dysphoria, Parenting Practice, and Grandchild Adjustment. Family Relations, 59(1), 45–59.
Smyke, A. T., Zeanah, C. H., Fox, N. A., Nelson, C. A., & Guthrie, D. (2010). Placement in foster care enhances quality of attachment among young institutionalized children. Child Development, 81(1), 212–223.
Spear, H. J. (2006). Breastfeeding behaviors and experiences of adolescent mothers. MCN: The American Journal of Maternal/Child Nursing, 31(2), 106–113.
Stronach, E. P., Toth, S. L., Rogosch, F., Oshri, A., Manly, J. T., & Cicchetti, D. (2011). Child maltreatment, attachment security, and internal representations of mother and mother-child relationships. Child Maltreatment, 16(2), 137–145.
Valiathan, R., Ashman, M., & Asthana, D. (2016). Effects of ageing on the immune system: infants to elderly. Scandinavian Journal of Immunology, 83(4), 255–266.
Walters, G. D. (2013). Drugs, crime, and their relationships: Theory, research, practice, and policy. Jones & Bartlett Publishers.
Ware, J. E., Kosinski, M., & Keller, S. D. (1994). SF-36 Physical and Mental Health Summary Scales: A Users' Manual. Boston: The Health Institute.
Wolff, M. S., & Ijzendoorn, M. H. (1997). Sensitivity and attachment: A meta-analysis on parental antecedents of infant attachment. Child Development, 68(4), 571–591.
Woods, J. A., Vieira, V. J., & Keylock, K. T. (2009). Exercise, inflammation, and innate immunity. Immunology and Allergy Clinics of North America, 29(2), 381–393.
Acknowledgements
The study was supported by a grant awarded to Nancy Schoenberg, Principle Investigator from the Retirement Research Foundation, an Igniting Research Collaborations grant awarded to Peggy S. Keller, Principle Investigator, and Nancy Schoenberg, Co-Investigator by the University of Kentucky, and a small grant awarded to Peggy S. Keller, Principle Investigator from the University of Kentucky Center for Clinical and Translational Science (CCTS). The CCTS is funded by the National Center for Advancing Translational Sciences, National Institutes of Health, through grant number UL1TR001998. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH or the Retirement Research Foundation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Disclosure of Interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Ethical Standards and Informed Consent
This study was conducted with the approval of the university Institutional Review Board; informed consent was obtained from grandparents and informed assent was obtained from grandchildren.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Keller, P.S., Bi, S. & Schoenberg, N. Children being Reared by their Grandparents in Rural Appalachia: A Pilot Study of Relations Between Psychosocial Stress and Changes in Salivary Markers of Inflammation Over Time. Journ Child Adol Trauma 12, 269–277 (2019). https://doi.org/10.1007/s40653-018-0214-z
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40653-018-0214-z